Tectothalamic inhibitory projection neurons in the avian torus semicircularis

Abstract

Inhibitory feedforward projection is one of key features of the organization of the central auditory system. In mammals, the inferior colliculus (IC) is the origin of a substantial inhibitory feedforward projection as well as an excitatory projection to the auditory thalamus. This inhibitory feedforward projection is provided by large γ-aminobutyric acid (GABA)ergic (LG) neurons, which are characterized by their receipt of dense excitatory axosomatic terminals positive for vesicular glutamate transporter (VGLUT) 2. In the avian torus semicircularis (TS), which is the homolog of the IC, neither the homology of cell types nor the presence of inhibitory feedforward inhibition have been established. In this study, we tested the presence of LG neurons in pigeon and chicken by neuroanatomical techniques. The TS contained two types of GABAergic neurons of different soma size. Of these, larger GABA + cells were encircled by dense VGLUT2 + axosomatic terminals. Ultrastructural analyses revealed that more than 30% of the perimeter of a large GABA+, but not small GABA + or GABA-, soma was covered by presumptive excitatory axosomatic terminals, suggesting that large GABA + cells are the sole recipient of dense excitatory axosomatic synapses. After injection of a retrograde tracer into the auditory thalamus, many retrogradely labeled neurons were found bilaterally in the TS, a few of which were GABA+. Almost all tectothalamic GABA + neurons had large somata, and received dense VGLUT2 + axosomatic terminals. These results clearly demonstrated the presence of LG neurons in birds. The similar morphology of LG neurons implies that the function of tectothalamic inhibition is similar among amniotes. J. Comp. Neurol. 524:2604-2622, 2016. © 2016 Wiley Periodicals, Inc.

Anatomical characterization of subcortical descending projections to the inferior colliculus in mouse

“…Electrical stimulation of the thalamus could trigger hyperpolarizing currents in the IC via collaterals of ascending tectothalamic inhibitory afferents, which would be antidromically activated after electrical stimulation. Although it is not known if such ascending GABAergic tectothalamic projections are present in the frog, they are found in both mammalian (Winer et al, 1996;Peruzzi et al, 1997;Venkataraman and Bartlett, 2013;Llano et al, 2014) and nonmammalian preparations (Ito and Atoji, 2016). In the visual system, an inhibitory projection from the pretectum to superior colliculus has been identified using both electrophysiological (Born and Schmidt, 2004) and anatomical (Appell and Behan, 1990;Kenigfest and Belekhova, 2009) methods.…”

Organization of subcortical auditory nuclei of Japanese house bat (Pipistrellus abramus) identified with cytoarchitecture and molecular expression

“…Therefore, GABAergic neurons likely act as hubs of sound information integration, which is required for echo analysis. Inside the amniote IC, two classes of GABAergic neurons are present, with large GABAergic (LG) cells receiving dense synaptic contacts from VGLUT2‐containing excitatory axosomatic terminals and project to the MGB, while small GABAergic (SG) cells lack dense axosomatic inputs (Ito et al, ; Ito & Atoji, ; Ito, Bishop, & Oliver, ; Ito & Oliver, ). LG cells receive converged inputs from ascending fibers from lower brainstem neurons (Ito et al, ) and collaterals from local neurons (Ito & Oliver, ).…”

Different coding strategy of sound information between GABAergic and glutamatergic neurons in the auditory midbrain

“…As shown in previous studies (Ito et al . ; Ito & Atoji, ), LG cells had the highest density of ExcAS terminals ( F (2,55) = 40.4, P < 0.001, ANOVA; Fig. 5).…”

“…13), confirming that LG cells are projection neurons (Ito et al . ; Ito & Atoji, ). In all of the LG cells, local axon collaterals were well developed.…”

“…1Bb and Cb), and on the distribution of VGLUT1&2-positive (+), markers of the GLU phenotype, axosomatic (AS) terminals (Ito et al 2009). In an optical section containing the nucleolus of a GABAergic neuron, we calculated the ratio of the total length of VGLUT1&2+ AS terminals to the perimeter of the soma, and the ratio of 0.3 was used as a threshold to distinguish LG and SG cells: a cell with ratio larger than 0.3 was categorized as a LG cell (Ito et al 2009;Ito & Atoji, 2016).…”